Top

Published in:

Open Access 01-04-2022 | Original Article

Dynamic Changes of NCR⁻ Type 3 Innate Lymphoid Cells and Their Role in Mice with Bronchopulmonary Dysplasia

Authors: Jiayu Cai, Hongyan Lu, Zhaoliang Su, Lanlan Mi, Suqing Xu, Zhengyang Xue

Published in: Inflammation | Issue 2/2022

Abstract—

Inflammation is one of the important pathogenesis of bronchopulmonary dysplasia (BPD). Type 3 innate lymphoid cells (ILC3) play a role in a variety of inflammatory lung diseases. In this study, we established the BPD model by injecting lipopolysaccharide into the amniotic cavity of pregnant mice. Here, we investigated the dynamic changes of ILC3 and NKP46⁻ ILC3 population in lung tissues of mice from BPD and the control groups. Results showed that the proportion of ILC3 and NKP46⁻ILC3 in the BPD group was higher than those of the control group. In addition, the cytokines interleukin-17 (IL-17) and interleukin-22 (IL-22) secreted by ILC3 in this model had also changed that their expression was significantly increased compared with that of the control group. Flow cytometry demonstrated that ILC3 were a rapid source of IL-17. In the anti-CD90 knockdown experiment, we confirmed the alleviation of BPD inflammation in the absence of ILC3. In addition, we injected mice with anti-IL-17 neutralizing antibody, and the results showed that IL-17 could aggravate BPD inflammation. Taken together, ILC3 may play a pro-inflammatory role in BPD by secreting IL-17.

Revhaug, C., M. Zasada, A.G.W. Rognlien, C.C. Gunther, A. Grabowska, T. Ksiazek, et al. 2020. Pulmonary vascular disease is evident in gene regulation of experimental bronchopulmonary dysplasia. The Journal of Maternal-Fetal & Neonatal Medicine 33 (12): 2122–2130. https://doi.org/10.1080/14767058.2018.1541081.CrossRef

Morty, R.E. 2018. Recent advances in the pathogenesis of BPD. Seminars in Perinatology 42 (7): 404–412. https://doi.org/10.1053/j.semperi.2018.09.001.CrossRefPubMed

Ruegger, C., M. Hegglin, M. Adams, H.U. Bucher, and N. Swiss Neonatal. 2012. Population based trends in mortality morbidity and treatment for very preterm- and very low birth weight infants over 12 years. BMC Pediatrics 12: 17. https://doi.org/10.1186/1471-2431-12-17.CrossRefPubMedPubMedCentral

Islam, J.Y., R.L. Keller, J.L. Aschner, T.V. Hartert, and P.E. Moore. 2015. Understanding the Short- and Long-Term Respiratory Outcomes of Prematurity and Bronchopulmonary Dysplasia. American Journal of Respiratory and Critical Care Medicine 192 (2): 134–156. https://doi.org/10.1164/rccm.201412-2142PP.CrossRefPubMedPubMedCentral

Ardain, A., J.Z. Porterfield, H.N. Kloverpris, and A. Leslie. 2019. Type 3 ILCs in Lung Disease. Frontiers in Immunology 10: 92. https://doi.org/10.3389/fimmu.2019.00092.CrossRefPubMedPubMedCentral

Bank, U., K. Deiser, C. Plaza-Sirvent, L. Osbelt, A. Witte, L. Knop, et al. 2020. c-FLIP is crucial for IL-7/IL-15-dependent NKp46(+) ILC development and protection from intestinal inflammation in mice. Nature Communications 11 (1): 1056. https://doi.org/10.1038/s41467-020-14782-3.CrossRefPubMedPubMedCentral

Entwistle, L.J., F. Puttur, L.G. Gregory, and C.M. Lloyd. 2020. Group 2 ILC Functional Assays in Allergic Airway Inflammation. Methods in Molecular Biology 2121: 99–114. https://doi.org/10.1007/978-1-0716-0338-3_10.CrossRefPubMed

Geremia, A., and C.V. Arancibia-Carcamo. 2017. Innate Lymphoid Cells in Intestinal Inflammation. Frontiers in Immunology 8: 1296. https://doi.org/10.3389/fimmu.2017.01296.CrossRefPubMedPubMedCentral

Reeves, R.K., K.C. De Grove, S. Provoost, F.M. Verhamme, K.R. Bracke, G.F. Joos, et al. 2016. Characterization and Quantification of Innate Lymphoid Cell Subsets in Human Lung. PLoS ONE 11 (1): e0145961. https://doi.org/10.1371/journal.pone.0145961.CrossRef

10.

Diefenbach, A., M. Colonna, and S. Koyasu. 2014. Development differentiation and diversity of innate lymphoid cells. Immunity 41 (3): 354–365. https://doi.org/10.1016/j.immuni.2014.09.005.CrossRefPubMedPubMedCentral

11.

Zeng, B., S. Shi, G. Ashworth, C. Dong, J. Liu, and F. Xing. 2019. ILC3 function as a double-edged sword in inflammatory bowel diseases. Cell Death & Disease 10 (4): 315. https://doi.org/10.1038/s41419-019-1540-2.CrossRef

12.

van de Pavert, S.A., and E. Vivier. 2016. Differentiation and function of group 3 innate lymphoid cells from embryo to adult. International Immunology 28 (1): 35–42. https://doi.org/10.1093/intimm/dxv052.CrossRefPubMed

13.

Rankin, L.C., M.J. Girard-Madoux, C. Seillet, L.A. Mielke, Y. Kerdiles, A. Fenis, et al. 2016. Complementarity and redundancy of IL-22-producing innate lymphoid cells. Nature Immunology 17 (2): 179–186. https://doi.org/10.1038/ni.3332.CrossRefPubMed

14.

Eken, A., A.K. Singh, P.M. Treuting, and M. Oukka. 2014. IL-23R+ innate lymphoid cells induce colitis via interleukin-22-dependent mechanism. Mucosal Immunology 7 (1): 143–154. https://doi.org/10.1038/mi.2013.33.CrossRefPubMed

15.

Song, C., J.S. Lee, S. Gilfillan, M.L. Robinette, R.D. Newberry, T.S. Stappenbeck, et al. 2015. Unique and redundant functions of NKp46+ ILC3s in models of intestinal inflammation. Journal of Experimental Medicine 212 (11): 1869–1882. https://doi.org/10.1084/jem.20151403.CrossRef

16.

Steigler, P., N.J. Daniels, T.R. McCulloch, B.M. Ryder, S.K. Sandford, and J.R. Kirman. 2018. BCG vaccination drives accumulation and effector function of innate lymphoid cells in murine lungs. Immunology and Cell Biology 96 (4): 379–389. https://doi.org/10.1111/imcb.12007.CrossRefPubMed

17.

Maertzdorf, J., M. Tonnies, L. Lozza, S. Schommer-Leitner, H. Mollenkopf, T.T. Bauer, et al. 2018. Mycobacterium tuberculosis Invasion of the Human Lung: First Contact. Frontiers in Immunology 9: 1346. https://doi.org/10.3389/fimmu.2018.01346.CrossRefPubMedPubMedCentral

18.

Everaere, L., S. Ait-Yahia, O. Molendi-Coste, H. Vorng, S. Quemener, P. LeVu, et al. 2016. Innate lymphoid cells contribute to allergic airway disease exacerbation by obesity. Journal of Allergy and Clinical Immunology 138 (5): 1309–1318. https://doi.org/10.1016/j.jaci.2016.03.019.CrossRef

19.

Ambigapathy, G., T. Schmit, R.K. Mathur, S. Nookala, S. Bahri, L.A. Pirofski, et al. 2019. Double-Edged Role of Interleukin 17A in Streptococcus pneumoniae Pathogenesis During Influenza Virus Coinfection. The Journal of Infectious Diseases 220 (5): 902–912. https://doi.org/10.1093/infdis/jiz193.CrossRefPubMedPubMedCentral

20.

Wu, Y., J. Yue, J. Wu, W. Zhou, D. Li, K. Ding, et al. 2018. Obesity May Provide Pro-ILC3 Development Inflammatory Environment in Asthmatic Children. Journal of Immunology Research 2018: 1628620. https://doi.org/10.1155/2018/1628620.CrossRefPubMedPubMedCentral

21.

Yanagisawa, H., M. Hashimoto, S. Minagawa, N. Takasaka, R. Ma, C. Moermans, et al. 2017. Role of IL-17A in murine models of COPD airway disease. American Journal of Physiology-Lung Cellular and Molecular Physiology 312 (1): L122–L130. https://doi.org/10.1152/ajplung.00301.2016.CrossRefPubMed

22.

Jonckheere, A.C., D.M.A. Bullens, and S.F. Seys. 2019. Innate lymphoid cells in asthma: Pathophysiological insights from murine models to human asthma phenotypes. Current Opinion in Allergy and Clinical Immunology 19 (1): 53–60. https://doi.org/10.1097/ACI.0000000000000497.CrossRefPubMed

23.

Xiong, H., W. Keith James, W. Samilo Dane, A. Carter Rebecca, M. Leiner Ingrid, and G. Pamer Eric. 2016. Innate Lymphocyte/Ly6C hi Monocyte Crosstalk Promotes Klebsiella Pneumoniae Clearance. Cell 165 (3): 679–689. https://doi.org/10.1016/j.cell.2016.03.017.CrossRefPubMedPubMedCentral

24.

Liu, M., Y. Zhao, C. Wang, H. Luo, A. Peng, and L. Ye. 2019. Interleukin-17 plays a role in pulp inflammation partly by WNT5A protein induction. Archives of Oral Biology 103: 33–39. https://doi.org/10.1016/j.archoralbio.2019.05.003.CrossRefPubMed

25.

Kim, J., Y. Chang, B. Bae, K.H. Sohn, S.H. Cho, D.H. Chung, et al. 2019. Innate immune crosstalk in asthmatic airways: Innate lymphoid cells coordinate polarization of lung macrophages. Journal of Allergy and Clinical Immunology 143 (5): 1769–1782. https://doi.org/10.1016/j.jaci.2018.10.040.CrossRef

26.

Cho, S.X., I. Rudloff, J.C. Lao, M.A. Pang, R. Goldberg, C.B. Bui, et al. 2020. Characterization of the pathoimmunology of necrotizing enterocolitis reveals novel therapeutic opportunities. Nature Communications 11 (1): 5794. https://doi.org/10.1038/s41467-020-19400-w.CrossRefPubMedPubMedCentral

27.

Liu, Y., Y. Song, D. Lin, L. Lei, Y. Mei, Z. Jin, et al. 2019. NCR(-) group 3 innate lymphoid cells orchestrate IL-23/IL-17 axis to promote hepatocellular carcinoma development. eBioMedicine 41: 333–344. https://doi.org/10.1016/j.ebiom.2019.02.050.CrossRefPubMedPubMedCentral

28.

Mazzurana, L., M. Forkel, A. Rao, A. Van Acker, E. Kokkinou, T. Ichiya, et al. 2019. Suppression of Aiolos and Ikaros expression by lenalidomide reduces human ILC3-ILC1/NK cell transdifferentiation. European Journal of Immunology 49 (9): 1344–1355. https://doi.org/10.1002/eji.201848075.CrossRefPubMed

29.

Mai, J., G. Nanayakkara, J. Lopez-Pastrana, X. Li, Y.F. Li, X. Wang, et al. 2016. Interleukin-17A Promotes Aortic Endothelial Cell Activation via Transcriptionally and Post-translationally Activating p38 Mitogen-activated Protein Kinase (MAPK) Pathway. Journal of Biological Chemistry 291 (10): 4939–4954. https://doi.org/10.1074/jbc.M115.690081.CrossRef

30.

Wang, Z., Y. Jia, F. Du, M. Chen, X. Dong, Y. Chen, et al. 2017. IL-17A Inhibits Osteogenic Differentiation of Bone Mesenchymal Stem Cells via Wnt Signaling Pathway. Medical Science Monitor 23: 4095–4101. https://doi.org/10.12659/msm.903027.CrossRefPubMedPubMedCentral

31.

Luo, J., X. An, Y. Yao, C. Erb, A. Ferguson, J.K. Kolls, et al. 2019. Epigenetic Regulation of IL-17-Induced Chemokines in Lung Epithelial Cells. Mediators of Inflammation 2019: 9050965. https://doi.org/10.1155/2019/9050965.CrossRefPubMedPubMedCentral

32.

Hanashiro, J., Y. Muraosa, T. Toyotome, K. Hirose, A. Watanabe, and K. Kamei. 2019. Schizophyllum commune induces IL-17-mediated neutrophilic airway inflammation in OVA-induced asthma model mice. Scientific Reports 9 (1): 19321. https://doi.org/10.1038/s41598-019-55836-x.CrossRefPubMedPubMedCentral

33.

Bayes, H.K., N.D. Ritchie, and T.J. Evans. 2016. Interleukin-17 Is Required for Control of Chronic Lung Infection Caused by Pseudomonas aeruginosa. Infection and Immunity 84 (12): 3507–3516. https://doi.org/10.1128/IAI.00717-16.CrossRefPubMedPubMedCentral

34.

Chuammitri, P., K. Wongsawan, K. Pringproa, and R. Thanawongnuwech. 2019. Interleukin 17 (IL-17) manipulates mouse bone marrow- derived neutrophils in response to acute lung inflammation. Comparative Immunology Microbiology and Infectious Diseases 67: 101356. https://doi.org/10.1016/j.cimid.2019.101356.CrossRef

35.

Kuwabara, T., F. Ishikawa, M. Kondo, and T. Kakiuchi. 2017. The Role of IL-17 and Related Cytokines in Inflammatory Autoimmune Diseases. Mediators of Inflammation 2017: 3908061. https://doi.org/10.1155/2017/3908061.CrossRefPubMedPubMedCentral

36.

Ma, W.T., K. Gu, R. Yang, X.D. Tang, Y.X. Qi, M.J. Liu, et al. 2020. Interleukin-17 mediates lung injury by promoting neutrophil accumulation during the development of contagious caprine pleuropneumonia. Veterinary Microbiology 243: 108651. https://doi.org/10.1016/j.vetmic.2020.108651.CrossRefPubMed

37.

Li, Y., Y. Shen, D. Lin, H. Zhang, T. Wang, H. Liu, et al. 2019. Neutrophils and IL17A mediate flagellar hook protein FlgE-induced mouse acute lung inflammation. Cellular Microbiology 21 (3): e12975. https://doi.org/10.1111/cmi.12975.CrossRefPubMed

38.

Zong, S., K. Li, G. Zeng, Y. Fang, and J. Zhao. 2016. The Effects of Interleukin-17 (IL-17)-Related Inflammatory Cytokines and A20 Regulatory Proteins on Astrocytes in Spinal Cord Cultured In Vitro. Cellular Physiology and Biochemistry 38 (3): 1100–1110. https://doi.org/10.1159/000443060.CrossRefPubMed

39.

Hebert, K.D., N. McLaughlin, M. Galeas-Pena, Z. Zhang, T. Eddens, A. Govero, et al. 2020. Targeting the IL-22/IL-22BP axis enhances tight junctions and reduces inflammation during influenza infection. Mucosal Immunology 13 (1): 64–74. https://doi.org/10.1038/s41385-019-0206-9.CrossRefPubMed

40.

Broquet, A., A. Besbes, J. Martin, C. Jacqueline, M. Vourc’h, A. Roquilly, et al. 2020. Interleukin-22 regulates interferon lambda expression in a mice model of pseudomonas aeruginosa pneumonia. Molecular Immunology 118: 52–59. https://doi.org/10.1016/j.molimm.2019.12.003.CrossRefPubMed

Title: Dynamic Changes of NCR− Type 3 Innate Lymphoid Cells and Their Role in Mice with Bronchopulmonary Dysplasia
Authors: Jiayu Cai
Hongyan Lu
Zhaoliang Su
Lanlan Mi
Suqing Xu
Zhengyang Xue
Publication date: 01-04-2022
Publisher: Springer US
Published in: Inflammation / Issue 2/2022
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI: https://doi.org/10.1007/s10753-021-01543-7

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Dynamic Changes of NCR⁻ Type 3 Innate Lymphoid Cells and Their Role in Mice with Bronchopulmonary Dysplasia

Abstract—

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract—

Please log in to get access to this content

Other articles of this Issue 2/2022

The Therapeutic Effect of an Anti-TNF-α/HSA/IL-6R Triple-Specific Fusion Protein Under Experimental Septic Conditions

CCAAT/Enhancer-Binding Protein Homologous Protein (CHOP) Deficiency Attenuates Heatstroke-Induced Intestinal Injury

Melatonin Attenuates Ropivacaine-Induced Apoptosis by Inhibiting Excessive Mitophagy Through the Parkin/PINK1 Pathway in PC12 and HT22 Cells

Unfractionated Heparin Attenuated Histone-Induced Pulmonary Syndecan-1 Degradation in Mice: a Preliminary Study on the Roles of Heparinase Pathway

Correction to: Human Saliva as a Diagnostic Specimen for Early Detection of Inflammatory Biomarkers by Real-time RT-PCR

Increased Plasma YKL-40 Level and Chitotriosidase Activity in Cystic Fibrosis Patients

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page